Demis Hassabis

Deconstructing episodic memory with construction

It has recently been observed that the brain network supporting recall of episodic memories shares much in common with other cognitive functions such as episodic future thinking, navigation and theory of mind. It has been speculated that self-projection is the key common process. However, in this Opinion article, we note that other functions (e.g. imagining fictitious experiences) not explicitly connected to either the self or a subjective sense of time, activate a similar brain network. Hence, we argue that the process of scene construction is better able to account for the commonalities in the brain areas engaged by an extended range of disparate functions. In light of this, we re-evaluate our understanding of episodic memory, the processes underpinning it and other related cognitive functions.

The Future of Memory: Remembering, Imagining, and the Brain

During the past few years, there has been a dramatic increase in research examining the role of memory in imagination and future thinking. This work has revealed striking similarities between remembering the past and imagining or simulating the future, including the finding that a common brain network underlies both memory and imagination. Here, we discuss a number of key points that have emerged during recent years, focusing in particular on the importance of distinguishing between temporal and nontemporal factors in analyses of memory and imagination, the nature of differences between remembering the past and imagining the future, the identification of component processes that comprise the default network supporting memory-based simulations, and the finding that this network can couple flexibly with other networks to support complex goal-directed simulations. This growing area of research has broadened our conception of memory by highlighting the many ways in which memory supports adaptive functioning.

When fear is near: Threat imminence elicits prefrontal-periaqueductal gray shifts in humans

Humans, like other animals, alter their behavior depending on whether a threat is close or distant. We investigated spatial imminence of threat by developing an active avoidance paradigm in which volunteers were pursued through a maze by a virtual predator endowed with an ability to chase, capture, and inflict pain. Using functional magnetic resonance imaging, we found that as the virtual predator grew closer, brain activity shifted from the ventromedial prefrontal cortex to the periaqueductal gray. This shift showed maximal expression when a high degree of pain was anticipated. Moreover, imminence-driven periaqueductal gray activity correlated with increased subjective degree of dread and decreased confidence of escape. Our findings cast light on the neural dynamics of threat anticipation and have implications for the neurobiology of human anxiety-related disorders.

Decoding Neuronal Ensembles in the Human Hippocampus

Summary Background The hippocampus underpins our ability to navigate, to form and recollect memories, and to imagine future experiences. How activity across millions of hippocampal neurons supports these functions is a fundamental question in neuroscience, wherein the size, sparseness, and organization of the hippocampal neural code are debated. Results Here, by using multivariate pattern classification and high spatial resolution functional MRI, we decoded activity across the population of neurons in the human medial temporal lobe while participants navigated in a virtual reality environment. Remarkably, we could accurately predict the position of an individual within this environment solely from the pattern of activity in his hippocampus even when visual input and task were held constant. Moreover, we observed a dissociation between responses in the hippocampus and parahippocampal gyrus, suggesting that they play differing roles in navigation. Conclusions These results show that highly abstracted representations of space are expressed in the human hippocampus. Furthermore, our findings have implications for understanding the hippocampal population code and suggest that, contrary to current consensus, neuronal ensembles representing place memories must be large and have an anisotropic structure.

Tracking the Emergence of Conceptual Knowledge during Human Decision Making

Summary Concepts lie at the very heart of intelligence, providing organizing principles with which to comprehend the world. Surprisingly little, however, is understood about how we acquire and deploy concepts. Here, we show that a functionally coupled circuit involving the hippocampus and ventromedial prefrontal cortex (vMPFC) underpins the emergence of conceptual knowledge and its effect on choice behavior. Critically, the hippocampus alone supported the efficient transfer of knowledge to a perceptually novel setting. These findings provide compelling evidence that the hippocampus supports conceptual learning through the networking of discrete memories and reveal the nature of its interaction with downstream valuation modules such as the vMPFC. Our study offers neurobiological insights into the remarkable capacity of humans to discover the conceptual structure of related experiences and use this knowledge to solve exacting decision problems.

Decoding Individual Episodic Memory Traces in the Human Hippocampus

Summary In recent years, multivariate pattern analyses have been performed on functional magnetic resonance imaging (fMRI) data, permitting prediction of mental states from local patterns of blood oxygen-level-dependent (BOLD) signal across voxels [1, 2]. We previously demonstrated that it is possible to predict the position of individuals in a virtual-reality environment from the pattern of activity across voxels in the hippocampus [3]. Although this shows that spatial memories can be decoded, substantially more challenging, and arguably only possible to investigate in humans [4], is whether it is feasible to predict which complex everyday experience, or episodic memory, a person is recalling. Here we document for the first time that traces of individual rich episodic memories are detectable and distinguishable solely from the pattern of fMRI BOLD signals across voxels in the human hippocampus. In so doing, we uncovered a possible functional topography in the hippocampus, with preferential episodic processing by some hippocampal regions over others. Moreover, our results imply that the neuronal traces of episodic memories are stable (and thus predictable) even over many re-activations. Finally, our data provide further evidence for functional differentiation within the medial temporal lobe, in that we show the hippocampus contains significantly more episodic information than adjacent structures.

Cortical midline involvement in autobiographical memory

Recollecting autobiographical memories of personal past experiences is an integral part of our everyday lives and relies on a distributed set of brain regions. Their occurrence externally in the real world (‘realness’) and their self-relevance (‘selfness’) are two defining features of these autobiographical events. Distinguishing between personally experienced events and those that happened to other individuals, and between events that really occurred and those that were mere figments of the imagination, is clearly advantageous, yet the respective neural correlates remain unclear. Here we experimentally manipulated and dissociated realness and selfness during fMRI using a novel paradigm where participants recalled self (autobiographical) and non-self (from a movie or television news clips) events that were either real or previously imagined. Distinct sub-regions within dorsal and ventral medial prefrontal cortex, retrosplenial cortex and along the parieto-occipital sulcus preferentially coded for events (real or imagined) involving the self. By contrast, recollection of autobiographical events that really happened in the external world activated different areas within ventromedial prefrontal cortex and posterior cingulate cortex. In addition, recall of externally experienced real events (self or non-self) was associated with increased activity in areas of dorsomedial prefrontal cortex and posterior cingulate cortex. Taken together our results permitted a functional deconstruction of anterior (medial prefrontal) and posterior (retrosplenial cortex, posterior cingulate cortex, precuneus) cortical midline regions widely associated with autobiographical memory but whose roles have hitherto been poorly understood.

Imagine All the People: How the Brain Creates and Uses Personality Models to Predict Behavior

The behaviors of other people are often central to envisioning the future. The ability to accurately predict the thoughts and actions of others is essential for successful social interactions, with far-reaching consequences. Despite its importance, little is known about how the brain represents people in order to predict behavior. In this functional magnetic resonance imaging study, participants learned the unique personality of 4 protagonists and imagined how each would behave in different scenarios. The protagonists personalities were composed of 2 traits: Agreeableness and Extraversion. Which protagonist was being imagined was accurately inferred based solely on activity patterns in the medial prefrontal cortex using multivariate pattern classification, providing novel evidence that brain activity can reveal whom someone is thinking about. Lateral temporal and posterior cingulate cortex discriminated between different degrees of agreeableness and extraversion, respectively. Functional connectivity analysis confirmed that regions associated with trait-processing and individual identities were functionally coupled. Activity during the imagination task, and revealed by functional connectivity, was consistent with the default network. Our results suggest that distinct regions code for personality traits, and that the brain combines these traits to represent individuals. The brain then uses this personality model to predict the behavior of others in novel situations.

Differential engagement of brain regions within a ‘core’ network during scene construction

Reliving past events and imagining potential future events engages a well-established “core” network of brain areas. How the brain constructs, or reconstructs, these experiences or scenes has been debated extensively in the literature, but remains poorly understood. Here we designed a novel task to investigate this (re)constructive process by directly exploring how naturalistic scenes are built up from their individual elements. We “slowed-down” the construction process through the use of auditorily presented phrases describing single scene elements in a serial manner. Participants were required to integrate these elements (ranging from three to six in number) together in their imagination to form a naturalistic scene. We identified three distinct sub-networks of brain areas, each with different fMRI BOLD response profiles, favouring specific points in the scene construction process. Areas including the hippocampus and retrosplenial cortex had a biphasic profile, activating when a single scene element was imagined and when 3 elements were combined together; regions including the intra-parietal sulcus and angular gyrus steadily increased activity from 1 to 3 elements; while activity in areas such as lateral prefrontal cortex was observed from the second element onwards. Activity in these sub-networks did not increase further when integrating more than three elements. Participants confirmed that three elements were sufficient to construct a coherent and vivid scene, and once this was achieved, the addition of further elements only involved maintenance or small changes to that established scene. This task offers a potentially useful tool for breaking down scene construction, a process that may be key to a range of cognitive functions such as episodic memory, future thinking and navigation.

Imagining fictitious and future experiences: Evidence from developmental amnesia

Research highlights ▶ Jon is a patient with developmental amnesia and bilateral hippocampal damage. ▶ Despite this, he is able to richly imagine fictitious and future scenarios. ▶ This is in contrast to most patients with adult-acquired amnesia. ▶ Residual hippocampal function may underpin preserved simulation ability.